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Lessons from Toads

John Pollack

May 1, 2002

Lessons from Toads

Carl Linneaus, the father of modern taxonomy, didn't think highly of toads. "These foul and loathsome animals are abhorrent because of their cold body, pale color, filthy skin, fierce aspect, calculating eye, offensive smell, harsh voice, squalid habitation, and terrible venom," he wrote of toads and other amphibians in 1758, "and so their Creator has not exerted his powers to make many of them."

Joseph Kiesecker

Frogs, toads, and other amphibians are very sensitive to their surroundings. They could be indicator species, warning of climate change.

He was wrong. Amphibians are abundant, noted biologist Joseph Kiesecker, in the fourth of this year's Penn State Lectures on the Frontiers of Science: Earth apparently holds as many of these "loathesome animals" as mammals. Taxonomists classify them into three orders: 160 species of caecilians, "wormlike, tropical amphibians that are very secretive" and little-known to science; 380 species of salamanders (the name means "fire lizard," since they often seemed to pop out of rotting logs when those were put on the fire) and newts; and 3,800 species of frogs and toads, several of which have gone extinct within a few years of their discovery, a fact disturbing to Kiesecker and other ecologists.

"Amphibians may be indicator species," said Kiesecker, a natural form of the "canary in the coal mine" warning of environmental stress. Because of their metamorphic life cycles—often, egg to tadpole (or other water-living larva) to land-based adult—amphibians need both aquatic and terrestrial habitats. Unlike birds or snakes, they lay eggs without shells. "The only thing protecting their eggs from the environment is a very thin and permeable gelatinous matrix." Even as adults, their moist skin, unprotected by scales or feathers or hair, is very sensitive to its surroundings.

Amphibians are also key elements in the food chain. Both predator and prey, they consume great quantities of insects, while themselves providing the exclusive food of many mammals, birds, and snakes. In fact, in some places they form the largest component of vertebrate biomass; that is, taken en masse, more live weight per acre is due to frogs, toads, salamanders, newts, and caecilians than to mammals, birds, or reptiles. "Their loss would have an effect," Kiesecker said.

So when reports of the decline of frogs and toads in relatively pristine environments such as nature reserves and parks began accumulating in the late 1980s, ecologists around the world became concerned. "We know that populations fluctuate naturally," Kiesecker said. "But here we were seeing mass mortality—losses of certain species across a wide geographical area." Habitat loss or the direct effects of pollution could not be the only answer in such wilderness sites. "The places in the West that have seen amphibian declines are not places that have overt signs of human effects. The changes aren't obvious, they're not things we can put our fingers on. Certain geographical areas seemed to be affected more than others, and even within those hot spots the declines didn't appear to be random."

Several of the species lost were new—and fascinating—to science. The strikingly colored Golden Toad, for example, was discovered in the Monteverdean Cloud Forest in Costa Rica in the mid-1970s. "By the mid-1980s, it was no longer found." A frog discovered near Queensland, Australia, in 1970 "had an amazing lifestyle," Kiesecker said. "When Mike Tyler, who discovered it, described the species, no one would believe him." The female swallows her eggs and broods them in her stomach until they hatch and the young emerge from her mouth. "The young release a chemical, a prostaglandin, that shuts off the mother's digestion," Kiesecker said. "This frog could have taught us a lot about digestive disorders, but it's no longer found." Since 1970, it has gone extinct.

"There's little consensus on the causes of these declines, but because they are on a global scale, we've started looking at global causes," Kiesecker said. In addition to habitat loss, suspects include an increase in ultraviolet radiation due to damage to the ozone layer by chlorofluorocarbons, changes in patterns of temperature and moisture, and outbreaks of disease.

"In the few places that have been examined in detail, we see a complicated mix of factors are responsible." Amphibians are thus a good example of how difficult it may be to understand how global climate change will translate into species loss in the future.

Kiesecker, for example, has been tracing outbreaks of disease in amphibians in the Cascade Mountains of Oregon. The Cascades frog, the western toad, and the Pacific tree frog had been studied for nearly 25 years prior to Kiesecker's study, giving him a good ground of baseline data. "We can find eggs of all three laid in one pond next to each other, yet we're losing the Cascades frog and the western toad, but not the Pacific tree frog."

Preliminary evidence from laboratory experiments led Kiesecker to suspect ultra-violet radiation was the cause. He took embryos of the Cascades frog, the western toad, and the Pacific tree frog and put them in enclosures. Some were protected from ultraviolet radiation, and others were not. Of the exposed embryos, only the Pacific tree frogs proved to be resistant to disease. The ultraviolet light, he determined, had stressed the embryos and damaged their DNA, making them more susceptible to infection. The tree frogs, however, had a better DNA-repair mechanism, particularly in terms of the activity of one enzyme called photolyase. Able to repair the damage, the tree frogs had stronger immune systems and could fight off infection.

"So exposure to ultraviolet radiation might be responsible for some of the mortality patterns," Kiesecker concluded. "But ecology is never that simple."

Joseph Kiesecker

Amphibians are going extinct in relatively pristine places, far from overt signs of human effects. Are we changing the environment in ways that promote disease?

As he and his colleagues continued to monitor the breeding sites for the declining Western toad, they expected to find that mortality would increase as the levels of ultraviolet light increased. They didn't. Instead of a change in the light, they discovered a change in the depth of the water of the embryos' natal ponds. "Some years, embryos developed in relatively deep water, and they developed normally. If they were in shallow water, the embryos did not develop normally." Through another experiment, he discovered that the water itself was shielding the embryos from ultraviolet radiation.

The next question was, what might be influencing the pattern of precipitation that determines the water levels in the ponds? The answer, Kiesecker discovered, has to do with the warming of sea surface temperatures in the South Pacific.

"It's known that for the Pacific Northwest, precipitation is related to the Southern Isolation Index, which in turn predicts El NiÃ±o events." In the Pacific Northwest, El NiÃ±o results in above-average temperatures and lower-than-normal precipitation. "So during El NiÃ±o years, embryos are exposed to low water levels and high ultra-violet radiation levels."

In another project, this time in central Pennsylvania, Kiesecker is investigating the association among disease, chemical pesticides and the gruesome deformities noticed in amphibians since the late 1980s. Frogs, toads, and other amphibians in 41 states in the U.S. have been found with missing legs, extra legs, and legs protruding from their backs or heads. The leading hypotheses are that the deformities are caused either by exposure to agricultural chemicals or as a response to infection.

Kiesecker has found it's a combination of both. As trees are cut down, the light that reaches ponds increases. More algae grows, which supports a larger snail population. The snails harbor one stage in the lifecycle of the trematode, a parasitic flatworm. The snails release a free-swimming trematode stage—what causes the rash known as "swimmer's itch" in humans. When these larval trematodes burrow into amphibian embryos, they form cysts that do more damage. In the presence of even very slight quantities of pesticides—equal to what's allowable under EPA drinking water standards—the embryo's immune system is suppressed. The cyst disturbs developing lim buds, resulting in deformed limbs and ultimately death of the growing amphibian.

As these investigations show, "no single explanation will explain amphibian declines," Kiesecker said. "Some form of climate change will influence disease outbreaks, but environmental stress is different in different geographic areas. What we're seeing is death by a thousand stings. Contaminants, ultraviolet radiation—all these things are acting in concert."

Yet there is an overall lesson to be learned. "Amphibian declines have caused us to focus on the effects of global change. Trends in amphibians parallel a disturbing trend in wildlife disease and also a trend in human disease, things like lyme disease or even Ebola," Kiesecker said. "Are we changing the environment in ways that might promote infection? The mysterious declines in amphibians represent only a small fraction of our actual losses. I tend to think I'm not a biologist, I'm a necrologist—I don't study life, I study death. Every year another population of amphibians winks out, especially in places like Central America and Australia. What can people do? People can attempt to conserve habitat in any way they can."

Joseph Kiesecker, Ph.D., is assistant professor of biology in the Eberly College of Science. His work was funded by the National Institutes of Health/National Science Foundation Panel on the Ecology of Infectious Diseases.